Measuring genome-wide genetic variation to reassess subspecies classifications in Dodonaea viscosa (Sapindaceae)
Matthew J. Christmas A , Ed Biffin B and Andrew J. Lowe C DA Department of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University,751 23, Uppsala, Sweden.
B State Herbarium of South Australia, Hackney Road, Adelaide, SA 5000, Australia.
C Environment Institute and School of Biological Sciences, The University of Adelaide, North Terrace, SA 5005, Australia.
D Corresponding author. Email: andrew.lowe@adelaide.edu.au
Australian Journal of Botany 66(4) 287-297 https://doi.org/10.1071/BT17046
Submitted: 21 March 2017 Accepted: 14 May 2018 Published: 9 July 2018
Abstract
Subspecies are traditionally defined on the basis of geographic discontinuities in phenotypic traits, and their circumscription is useful to distinguish morphologically differentiated populations. However, the robustness of morphology-based subspecies classifications in the genomics era is coming under increasing scrutiny, and phylogenies inferred from molecular data may not match with morphological approaches. The division of the shrub Dodonaea viscosa into seven subspecies within Australia has been based mainly on variation in leaf shape, which is a notably variable phenotypic character in this species. So as to assess the alignment between genetic variation and subspecies assignment, we genotyped 67 D. viscosa plants, including representatives from each of the seven subspecies, for 941 single nucleotide polymorphisms. We used network- and Bayesian-based methods to assess genetic relatedness between sampled individuals. Structure analysis identified two genetic clusters, with a further substructure being identified within one of the clusters. Genetic clusters partially aligned with subspecies classifications, particularly for the three most morphologically distinct subspecies (ssp. mucronata, ssp. viscosa and ssp. burmanniana). Subspecies inhabiting the arid zone (ssp. mucronata and ssp. angustissima) exhibited the most distinct genetic clustering. For subspecies inhabiting more temperate regions of its range (ssp. angustifolia, ssp. cuneata and ssp. spatulata), genetic groups did not correspond well with subspecies classifications, but rather were better explained by the geographic origin of individuals. We suggest that the current subspecific classification of the hopbush does not accurately reflect the evolutionary history of this species, and recommend that phenotypic variation be reassessed in light of the genetic structure we describe here. The roles of environmental change, selection and geographic isolation are discussed in an attempt to explain the contemporary distribution of genetic variation in D. viscosa in Australia.
References
Baruch Z, Christmas MJ, Breed MF, Guerin GR, Caddy‐Retalic S, McDonald J, Jardine DI, Leitch E, Gellie N, Hill K, McCallum K, Lowe AJ (2017) Leaf trait associations with environmental variation in the wide‐ranging shrub Dodonaea viscosa subsp. angustissima (Sapindaceae). Austral Ecology 42, 553–561.| Leaf trait associations with environmental variation in the wide‐ranging shrub Dodonaea viscosa subsp. angustissima (Sapindaceae).Crossref | GoogleScholarGoogle Scholar |
Bennett JR, Wood JR, Scotland RW (2008) Uncorrelated variation in widespread species: species delimitation in Strobilanthes echinata Nees (Acanthaceae). Botanical Journal of the Linnean Society 156, 131–141.
| Uncorrelated variation in widespread species: species delimitation in Strobilanthes echinata Nees (Acanthaceae).Crossref | GoogleScholarGoogle Scholar |
Bentham G (1863–1878) ‘Flora Australiensis: a description of the plants of the Australian Territory.’ (Lovell Reeve: London)
Bird KA, An H, Gazave E, Gore MA, Pires JC, Robertson LD, Labate JA (2017) Population structure and phylogenetic relationships in a diverse panel of Brassica rapa L. Frontiers in Plant Science 8, 321
| Population structure and phylogenetic relationships in a diverse panel of Brassica rapa L.Crossref | GoogleScholarGoogle Scholar |
Bowler J (1982) Aridity in the late Tertiary and Quaternary of Australia. In ‘Evolution of the flora and fauna of arid Australia’. (Eds WR Barker, PJM Greenslade) pp. 35–45. (Peacock Publications: Adelaide)
Brandrud MK, Paun O, Lorenzo MT, Nordal I, Brysting AK (2017) RADseq provides evidence for parallel ecotypic divergence in the autotetraploid Cochlearia officinalis in Northern Norway. Scientific Reports 7, 5573
| RADseq provides evidence for parallel ecotypic divergence in the autotetraploid Cochlearia officinalis in Northern Norway.Crossref | GoogleScholarGoogle Scholar |
Bryant D, Moulton V (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Molecular Biology and Evolution 21, 255–265.
| Neighbor-net: an agglomerative method for the construction of phylogenetic networks.Crossref | GoogleScholarGoogle Scholar |
Christmas MJ, Biffin E, Breed MF, Lowe AJ (2016) Finding needles in a genomic haystack: targeted capture identifies clear signatures of selection in a nonmodel plant species. Molecular Ecology 25, 4216–4233.
| Finding needles in a genomic haystack: targeted capture identifies clear signatures of selection in a nonmodel plant species.Crossref | GoogleScholarGoogle Scholar |
Christmas MJ, Biffin E, Breed MF, Lowe AJ (2017) Targeted capture to assess neutral genomic variation in the narrow-leaf hopbush across a continental biodiversity refugium. Scientific Reports 7, 41367
| Targeted capture to assess neutral genomic variation in the narrow-leaf hopbush across a continental biodiversity refugium.Crossref | GoogleScholarGoogle Scholar |
Cross H, Biffin E, Lowe A, Waycott M (2016) Effective application of next-generation sequencing (NGS) approaches in systematics and population genetics: case studies in Eucalyptus and Acacia. Australian Systematic Botany 29, 235–246.
| Effective application of next-generation sequencing (NGS) approaches in systematics and population genetics: case studies in Eucalyptus and Acacia.Crossref | GoogleScholarGoogle Scholar |
Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nature Reviews Genetics 12, 499–510.
| Genome-wide genetic marker discovery and genotyping using next-generation sequencing.Crossref | GoogleScholarGoogle Scholar |
DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, Del Angel G, Rivas MA, Hanna M, McKenna A (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics 43, 491–498.
| A framework for variation discovery and genotyping using next-generation DNA sequencing data.Crossref | GoogleScholarGoogle Scholar |
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
| STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |
Edwards DL, Roberts J, Keogh JS (2007) Impact of Plio‐Pleistocene arid cycling on the population history of a southwestern Australian frog. Molecular Ecology 16, 2782–2796.
| Impact of Plio‐Pleistocene arid cycling on the population history of a southwestern Australian frog.Crossref | GoogleScholarGoogle Scholar |
Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, Holzapfel CM (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proceedings of the National Academy of Sciences of the United States of America 107, 16196–16200.
| Resolving postglacial phylogeography using high-throughput sequencing.Crossref | GoogleScholarGoogle Scholar |
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
| Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar |
Foote AD, Liu Y, Thomas GWC, Vinař T, Alföldi J, Deng J, Dugan S, van Elk CE, Hunter ME, Joshi V, Khan Z, Kovar C, Lee SL, Lindblad-Toh K, Mancia A, Nielsen R, Qin X, Qu J, Raney BJ, Vijay N, Wolf JBW, Hahn MW, Muzny DM, Worley KC, Gilbert MTP, Gibbs RA (2015) Convergent evolution of the genomes of marine mammals. Nature Genetics 47, 272–275.
| Convergent evolution of the genomes of marine mammals.Crossref | GoogleScholarGoogle Scholar |
Gentilli J (1971) Dynamics of the Australian troposphere. In ‘World survey of climatology: climates of Australia and New Zealand’. (Ed. J. Gentilli) pp. 53–117. (Elsevier: The Netherlands)
Gohli J, Leder E, Garcia‐del‐Rey E, Johannessen LE, Johnsen A, Laskemoen T, Popp M, Lifjeld JT (2015) The evolutionary history of Afrocanarian blue tits inferred from genome‐wide SNPs. Molecular Ecology 24, 180–191.
| The evolutionary history of Afrocanarian blue tits inferred from genome‐wide SNPs.Crossref | GoogleScholarGoogle Scholar |
Guerin GR, Lowe AJ (2012) Leaf morpholgy shift: new data and analysis support climate link. Biology Letters
| Leaf morpholgy shift: new data and analysis support climate link.Crossref | GoogleScholarGoogle Scholar |
Guerin GR, Wen H, Lowe AJ (2012) Leaf morphology shift linked to climate change. Biology Letters 8, 882–886.
| Leaf morphology shift linked to climate change.Crossref | GoogleScholarGoogle Scholar |
Harrington MG, Gadek PA (2009) A species well travelled: the Dodonaea viscosa (Sapindaceae) complex based on phylogenetic analyses of nuclear ribosomal ITS and ETSf sequences. Journal of Biogeography 36, 2313–2323.
| A species well travelled: the Dodonaea viscosa (Sapindaceae) complex based on phylogenetic analyses of nuclear ribosomal ITS and ETSf sequences.Crossref | GoogleScholarGoogle Scholar |
Hill KE, Guerin GR, Hill RS, Watling JR (2015) Temperature influences stomatal density and maximum potential water loss through stomata of Dodonaea viscosa subsp. angustissima along a latitude gradient in southern Australia. Australian Journal of Botany 62, 657–665.
| Temperature influences stomatal density and maximum potential water loss through stomata of Dodonaea viscosa subsp. angustissima along a latitude gradient in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S, Auton A, Muliyati NW, Platt A, Sperone FG, Vilhjálmsson BJ, Nordborg M (2012) Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nature Genetics 44, 212–216.
| Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel.Crossref | GoogleScholarGoogle Scholar |
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23, 254–267.
| Application of phylogenetic networks in evolutionary studies.Crossref | GoogleScholarGoogle Scholar |
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806.
| CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure.Crossref | GoogleScholarGoogle Scholar |
Joly S, Bryant DJ, Lockhart PJ (2015) Flexible methods for estimating genetic distances from single nucleotide polymorphisms. Methods in Ecology and Evolution 6, 938–948.
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405.
| adegenet: a R package for the multivariate analysis of genetic markers.Crossref | GoogleScholarGoogle Scholar |
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics 11, 94
| Discriminant analysis of principal components: a new method for the analysis of genetically structured populations.Crossref | GoogleScholarGoogle Scholar |
Mayr E (1982) Of what use are subspecies? The Auk 99, 593–595.
Mayr E, Ashlock PD (1991) ‘Principles of systematic biology.’ (McGraw-Hill: New York)
McCormack JE, Hird SM, Zellmer AJ, Carstens BC, Brumfield RT (2013) Applications of next-generation sequencing to phylogeography and phylogenetics. Molecular Phylogenetics and Evolution 66, 526–538.
| Applications of next-generation sequencing to phylogeography and phylogenetics.Crossref | GoogleScholarGoogle Scholar |
McLean C, Stuart‐Fox D, Moussalli A (2014) Phylogeographic structure, demographic history and morph composition in a colour polymorphic lizard. Journal of Evolutionary Biology 27, 2123–2137.
| Phylogeographic structure, demographic history and morph composition in a colour polymorphic lizard.Crossref | GoogleScholarGoogle Scholar |
Miller P (1754) ‘The gardener’s dictionary containing the methods of cultivating and improving all sorts of trees, plants and flowers.’ 4th edn. (Rivington: London)
Neaves LE, Zenger KR, Prince RI, Eldridge MD (2012) Impact of Pleistocene aridity oscillations on the population history of a widespread, vagile Australian mammal, Macropus fuliginosus. Journal of Biogeography 39, 1545–1563.
| Impact of Pleistocene aridity oscillations on the population history of a widespread, vagile Australian mammal, Macropus fuliginosus.Crossref | GoogleScholarGoogle Scholar |
Phillimore AB, Owens IPF (2006) Are subspecies useful in evolutionary and conservation biology? Proceedings. Biological Sciences 273, 1049–1053.
| Are subspecies useful in evolutionary and conservation biology?Crossref | GoogleScholarGoogle Scholar |
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Radlkofer L (1900) Sapindaceae. Flora Brasiliensis 13, 639–645.
Radlkofer L (1933) ‘Sapindaceae.’ (Verlag von Wilhelm Engelmann: Leipzig, Germany)
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.
Sakaguchi S, Bowman DM, Prior LD, Crisp MD, Linde CC, Tsumura Y, Isagi Y (2013) Climate, not Aboriginal landscape burning, controlled the historical demography and distribution of fire-sensitive conifer populations across Australia. Proceedings of the Royal Society of London. Series B, Biological Sciences 280, 20132182
| Climate, not Aboriginal landscape burning, controlled the historical demography and distribution of fire-sensitive conifer populations across Australia.Crossref | GoogleScholarGoogle Scholar |
Sherff EE (1945) Some additions to the genus Dodonaea L. (Fam. Sapindaceae). American Journal of Botany 32, 202–214.
| Some additions to the genus Dodonaea L. (Fam. Sapindaceae).Crossref | GoogleScholarGoogle Scholar |
Sherff EE (1947) Further studies in the genus Dodonaea L. (family Sapindaceae). Field Museum Natural History Botanical Series 23, 269–317.
Toon A, Mather PB, Baker AM, Durrant KL, Hughes JM (2007) Pleistocene refugia in an arid landscape: analysis of a widely distributed Australian passerine. Molecular Ecology 16, 2525–2541.
| Pleistocene refugia in an arid landscape: analysis of a widely distributed Australian passerine.Crossref | GoogleScholarGoogle Scholar |
Verdu CF, Guichoux E, Quevauvillers S, De Thier O, Laizet YH, Delcamp A, Gévaudant F, Monty A, Porté AJ, Lejeune P, Lassois L (2016) Dealing with paralogy in RADseq data: in silico detection and single nucleotide polymorphism validation in Robinia pseudoacacia L. Ecology and Evolution 6, 7323–7333.
| Dealing with paralogy in RADseq data: in silico detection and single nucleotide polymorphism validation in Robinia pseudoacacia L.Crossref | GoogleScholarGoogle Scholar |
Weber LC, VanDerWal J, Schmidt S, McDonald WJ, Shoo LP (2014) Patterns of rain forest plant endemism in subtropical Australia relate to stable mesic refugia and species dispersal limitations. Journal of Biogeography 41, 222–238.
| Patterns of rain forest plant endemism in subtropical Australia relate to stable mesic refugia and species dispersal limitations.Crossref | GoogleScholarGoogle Scholar |
West JG (1980) A taxonomic revision of Dodonaea (Sapindaceae) in Australia. PhD Thesis, University of Adelaide.
West JG (1982) Radiation and adaptation of Dodonaea (Sapindaceae) in arid Australia. In ‘Evolution of the flora and fauna of arid Australia’. (Eds W Barker, P Greenslade) pp. 329–333. (Peacock Publications: Adelaide)
West JG (1984) A revision of Dodonaea Miller (Sapindaceae) in Australia. Brunonia 7, 1–194.
| A revision of Dodonaea Miller (Sapindaceae) in Australia.Crossref | GoogleScholarGoogle Scholar |
West J, Noble I (1984) Analyses of digitised leaf images of the Dodonaea viscosa complex in Australia. Taxon 33, 595–613.
| Analyses of digitised leaf images of the Dodonaea viscosa complex in Australia.Crossref | GoogleScholarGoogle Scholar |
Wheeler M, Byrne M (2006) Congruence between phylogeographic patterns in cpDNA variation in Eucalyptus marginata (Myrtaceae) and geomorphology of the Darling Plateau, south-west of Western Australia. Australian Journal of Botany 54, 17–26.
| Congruence between phylogeographic patterns in cpDNA variation in Eucalyptus marginata (Myrtaceae) and geomorphology of the Darling Plateau, south-west of Western Australia.Crossref | GoogleScholarGoogle Scholar |